NAP1 catalyzes the formation of either positive or negative supercoils on DNA on basis of the dimer-tetramer equilibrium of histones H3/H4

Biochemistry

Volumn 46, Issue 29, 2007, Pages 8634-8646

  Peterson, Sharon ^a   Danowit, Rachel ^a   Wunsch, Ann ^a   Jackson, Vaughn ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE CHAPERONE; NUCLEOSOME ASSEMBLY PROTEIN 1 (NAP1); TETRAMER-DIMER EQUILIBRIUM;

CATALYSIS; CONFORMATIONS; DEPOSITION; DIMERS; DNA; FORMALDEHYDE; KETONES;

PROTEINS;

5,5' DITHIOBIS(2 NITROBENZOIC ACID); CHAPERONE; CYSTEINE; DIMER; HISTONE H3; HISTONE H4; NUCLEOSOME ASSEMBLY PROTEIN 1; PROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; DNA CROSS LINKING; DNA SUPERCOILING; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

CATALYSIS; CELL CYCLE PROTEINS; DIMERIZATION; DITHIONITROBENZOIC ACID; DNA, SUPERHELICAL; HISTONES; INDOLEACETIC ACIDS; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION;

EID: 34547126205     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi6025215     Document Type: Article

References (78)

1. Arents, G., Burlingame, R. W., Wang, B., Love, W. E., and Moudrianakis, E. N. (1991) The nucleosomal core histone octamer at 3.1 Å resolution: a tripartite protein assembly and a left-handed superhelix, Proc. Natl. Acad. Sci. U.S.A. 88, 10148-10152.
2. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution, Nature 389, 251-260.
3. Harp, J. M., Hanson, B. L., Timm, D. E., and Bunick, G. J. (2000) Asymmetries in the nucleosome core particle at 2.5 Å resolution, Acta Crystallogr. Sect. D 56, 1513-1534.
4. Germond, J. E., Hirt, B., Oudet, P., Gross-Bellark, M., and Chambon, P. (1975) Folding of the DNA double helix in chromatin-like structures from simian virus 40, Proc. Natl. Acad. Sci. U.S.A. 72, 1843-1847.
5. Hansen, J. C. (2002) Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions, Annu. Rev. Biophys. Biomol. Struct. 31, 361-392.
6. 2: a case of a mixed-associating system, Biochemistry 19, 1339-1346.
7. 2 system, Biochemistry 35, 2037-2046.
8. 2 histone tetramer of the core nucleosome, Protein Sci. 13, 1304-1316.
9. Banks, D. D., and Gloss, L. M. (2003) Equilibrium folding of the core histones: the H3-H4 tetramer is less stable than the H2A-H2B dimer, Biochemistry 42, 6827-6839.
10. Ruiz-Carrillo, A., and Jorcano, J. L. (1979) An octamer of core histones in solution: central role of the H3-H4 tetramer in the self-assembly, Biochemistry 18, 760-768.
11. Smith, S., and Stillman, B. (1991) Stepwise assembly of chromatin during DNA replication in vitro, EMBO J. 10, 971-980.
12. Tagami, H., Ray-Gallet, D., Almouzni, G., and Nakatani, Y. (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis, Cell 116, 51-61.
13. English, C. M., Maluf, N. K., Tripet, B., Churchill, M. E., and Tyler, J. K. (2005) ASF1 binds to a heterodimer of histones H3 and H4: A two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA, Biochemistry 44, 13673-13682.
14. Mousson, F., Lautrette, A., Thuret, J-Y., Agez, M., Courbeyrette, R., Amigues, B., Becker, E., Neumann, J-M., Guerois, R., Mann, C., and Ochsenbein, F. (2005) Structural basis for the interaction of Asf1 with histone H3 and its functional implications, Proc. Natl. Acad. Sci. U.S.A. 102, 5975-5980.
15. Daganzo, S. M., Erzberger, J. P., Lam, W. M., Skordalakes, E., Zhang, R., Franco, A. A., Brill, S. J., Adams, P. D., Berger, J. M., and Kaufman, P. D. (2003) Structure and function of the conserved core of histone deposition protein Asf1, Curr. Biol. 13, 2148-2158.
16. Ito, T., Bulger, M., Kobayashi, R., and Kadonaga, J. T. (1996) Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays, Mol. Cell Biol. 16, 3112-3124.
17. Chang, L., Loranger, S. S., Mizzen, C., Ernst, S. G., Allis, C. D., and Annunziato, A. T. (1997) Histones in transit: cytosolic histone complexes and diacetylation of H4 during nucleosome assembly in human cells, Biochemistry 36, 469-480.
18. Mosammaparast, N., Ewart, C. S., and Pemberton, L. F. (2002) A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B, EMBO J. 23, 6527-6538.
19. Zlatanova, J., Seebart, C., and Tomschik, M. (2007) Nap1: taking a closer look at a juggler protein of extraordinary skills, FASEB J. 21, 1294-1310.
20. 2 tetramer by NAP1 is mediated by the amino-terminal histone tails, J. Biol. Chem. 278, 44574-44583.
21. Ishimi, Y., Yasuda, H., Hirosumi, J., Hanaoka, F., and Yamada, M. (1983) A protein which facilitates assembly of nucleosome-like structures in vitro in mammalian cells, J. Biochem. (Tokyo) 94, 735-744.
22. Fujii-Nakata, T., Ishimi, Y., Okuda, A., and Kikuchi, A. (1992) Functional analysis of nucleosome assembly protein, NAP-1. The negatively charged COOH-terminal region is not necessary for the intrinsic assembly activity, J. Biol. Chem. 267, 20980-20986.
23. Nakagawa, T., Bulger, M., Muramatsu, M., and Ito, T. (2001) Multistep chromatin assembly on supercoiled plasmid DNA by nucleosome assembly protein-1 and ATP-utilizing chromatin assembly and remodeling factor, J. Biol. Chem. 276, 27384-27391.
24. Mazurkiewicz, J., Kepert, J. F., and Rippe, K. (2006) On the mechanism of nucleosome assembly by histone chaperone NAP1, J. Biol. Chem. 281, 16462-16472.
25. Walter, P. P., Owen-Hughes, T. A., Cote, J., and Workman, J. L. (1995) Stimulation of transcription factor binding and histone displacement by nucleosome assembly protein 1 and nucleoplasmin requires disruption of the histone octamer, Mol. Cell. Biol. 15, 6178-6187.
26. Ito, T., Ikehara, T., Nakagawa, T., Kraus, W. L., and Muramatsu, M. (2000) p300-Mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone, Genes Dev. 14, 1899-1907.
27. Asahara, H., Tartare-Deckert, S., Nakagawa, T., Ikehara, T., Hirose, F., Hunter, T., Ito, T., and Montminy, M. (2002) Dual roles of p300 in chromatin assembly and transcriptional activation in cooperation with nucleosome assembly protein 1 in vitro, Mol. Cell. Biol. 22, 2974-2983.
28. Rehtanz, M., Schmidt, H-M., Warthorst, U., and Steger, G. (2004) Direct interaction between nucleosome assembly protein 1 and the papillomavirus E2 proteins involved in activation of transcription, Mol. Cell. Biol. 24, 2153-2168.
29. Bruno, M., Flaus, A., Stockdale, C., Rencurel, C., Ferreira, H., and Owen-Hughes, T. (2003) Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodeling activities, Mol. Cell 12, 1599-1606.
30. Okuwaki, M., Kato, K., Shimahara, H., Tate, S., and Nagata, K. (2005) Assembly and disassembly of nucleosome core particles containing histone variants by human nucleosome assembly protein 1, Mol. Cell. Biol. 25, 10639-10651.
31. Lorch, Y., Maier-Davis, B., and Kornberg, R. D. (2006) Chromatin remodeling by nucleosome disassembly in vitro, Proc. Natl. Acad. Sci. U.S.A. 103, 3090-3093.
32. Levchenko, V., Jackson, B., and Jackson, V. (2005) Histone release during transcription: displacement of the two H2A-H2B dimers in the nucleosome is dependent on different levels of transcription-induced positive stress, Biochemistry 44, 5357-5372.
33. Flaus, A., and Owen-Hughes, T. (2004) Mechanisms of ATP-dependent chromatin remodeling: farewell to the tuna-can octamer?, Curr. Opin. Genet. Dev. 14, 165-173.
34. Jin, J., Cai, Y., Li, B., Conaway, R. C., Workman, J. L., Conaway, J. W., and Kusch, T. (2005) In and out: histone variant exchange in chromatin, Trends Biochem. Sci. 30, 680-687.
35. Benson, L. J., Gu, Y., Yakovleva, T., Tong, K., Barrows, C., Strack, C. L., Cook, R. G., Mizzen, C. A., and Annunziato, A. T. (2006) Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange, J. Biol. Chem. 281, 9287-9296.
36. Park, Y.-P., Chodaparambil, J. V., Bao, Y., McBryant, S. J., and Luger, K. (2005) Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding, J. Biol. Chem. 280, 1817-1825.
37. Ohkuni, K., Shirahige, K., and Kikuchi, A. (2003) Genome-wide expression analysis of NAP1 in Saccharomyces cerevisiae, Biochem. Biophys., Res. Commun. 306, 5-9.
38. 2 tetramer of the nucleosome with positively supercoiled DNA minicircles: potential flipping of the protein from a left-handed to a right-handed superhelical form, Proc. Natl. Acad. Sci. U.S.A. 93, 7588-7593.
39. 2 tetramer-DNA particle, J. Mol. Biol. 291, 815-841.
40. 2 tetramer within a nucleoprotein particle requires a reorientation of the H3-H3 interface, J. Biol. Chem. 273, 9261-9269.
41. Liu, L. F., and Wang, J. C. (1987) Supercoiling of the DNA template during transcription, Proc. Natl. Acad. Sci. U.S.A. 84, 7024-7027.
42. Rahmouni, A. R., and Wells, R. D. (1992) Direct evidence for the effect of transcription on local DNA supercoiling in vivo, J. Mol. Biol. 223, 131-144.
43. Kramer, P. R., and Sinden, R. R. (1997) Measurement of unrestrained negative supercoiling and topological domain size in living human cells, Biochemistry 36, 3151-3158.
44. Wang, Z., and Droge, P. (1997) Long-range effects in a supercoiled DNA domain generated by transcription in vitro, J. Mol. Biol. 271, 499-510.
45. Peng, H. F., and Jackson, V. (2000) In vitro studies on the maintenance of transcription-induced stress by histones and polyamines, J. Biol. Chem. 275, 657-668.
46. Simon, R. H., and Felsenfeld, G. (1979) A new procedure for purifying histone pairs H2A + H2B and H3 + H4 from chromatin using hydroxylapatite, Nucleic Acids Res. 6, 689-696.
47. Stein, A. (1979) DNA folding by histones: The kinetics of chromatin core particle reassembly and the interaction of nucleosomes with histones, J. Mol. Biol. 130, 103-134.
48. Ausio, J., Dong, F., and van Holde, K. E. (1989) Use of selectively trypsinized nucleosome core particles to analyze the role of the histone 'tails' in the stabilization of the nucleosome, J. Mol. Biol. 206, 451-463.
49. Bohm, L, Briand, G., Sautiere, P., and Crane-Robinson, C. (1981) Proteolytic digestion studies of chromatin core-histone structure: Identification of the limit peptides of histones H3 and H4, Eur. J. Biochem. 119, 67-74.
50. Pfaffle, P., and Jackson, V. (1990) Studies on rates of nucleosome formation with DNA under stress, J. Biol. Chem. 265, 16821-16829.
51. Liu, L. F., and Miller, K. G. (1981) Eukaryotic DNA topoisomerases: two forms of type I DNA topoisomerases from HeLa cell nuclei, Proc. Natl. Acad. Sci. U.S.A. 78, 3487-3491.
52. Edelhoch, H. (1967) Spectroscopic determination of tryptophan and tyrosine in proteins, Biochemistry 6, 1948-1954.
53. McBryant, S. J., and Peersen, O. B. (2004) Self-association of the yeast nucleosome assembly protein 1, Biochemistry 43, 10592-10599.
54. Depew, R. E., and Wang, J. C. (1975) Conformational fluctuations of DNA helix, Proc. Natl. Acad. Sci. U.S.A. 72, 4275-4279.
55. Anderson, P., and Bauer, W. (1978) Supercoiling in closed circular DNA: dependence upon ion type and concentration, Biochemistry 17, 594-601.
56. O'Neill, T. E., Smith, J. G., and Bradbury, E. M. (1993) Histone octamer dissociation is not required for transcript elongation through arrays of nucleosome cores by phage T7 RNA polymerase in vitro, Proc. Natl. Acad. Sci. U.S.A. 90, 6203-6207.
57. Jackson, S., Brooks, W., and Jackson, V. (1994) Dynamics of the interactions of histones H2A, H2B and H3, H4 with torsionally stressed DNA, Biochemistry 33, 5392-5403.
58. Jackson, V. (1978) Studies on histone organization in the nucleosome using formaldehyde as a reversible cross-linking agent, Cell 15, 945-954.
59. Ruiz-Carrillo, A., Jorcano, J. L., Eder, G., and Lurz, R. (1979) In vitro core particle and nucleosome assembly at physiological ionic strength, Proc. Natl. Acad. Sci. U.S.A. 76, 3284-3288.
60. Daban, J-R., and Cantor, C. R. (1982) Structural and kinetic study of the self assembly of nucleosome core particles, J. Mol. Biol. 156, 749-769.
61. Diaz, P., and Daban, J-R. (1986) Nucleosome core particle self-assembly kinetics and stability at physiological ionic strength, Biochemistry 25, 7736-7744.
62. Aragay, A. M., Diaz, P., and Daban, J-R. (1988) Association of nucleosome core particle DNA with different histone oligomers: transfer of histones between DNA-(H2A, H2B) and DNA-(H3, H4) complexes, J. Mol. Biol. 204, 141-154.
63. Wagner, G., Bancaud, A., Quivy, J-P., Clapier, C., Almouzni, G., and Viovy, J-L. (2005) Compaction kinetics on single DNAs: purified nucleosome reconstitution systems versus crude extract, Biophys. J. 89, 3647-3659.
64. Zheng, C., Lu, X., Hansen, J. C., and Hayes, J. J. (2005) Salt-dependent intra- and internucleosomal interactions of the H3 tail domain in a model oligonucleosomal array, J. Biol. Chem. 280, 33552-33557.
65. Widlund, H. R., Vitolo, J. M., Thiriet, C., and Hayes, J. J. (2000) DNA sequence-dependent contributions of core histone tails to nucleosome stability: differential effects of acetylation and proteolytic tail removal, Biochemistry 39, 3835-3841.
66. Garcia-Ramirez, M., Dong, F., and Ausio, J. (1992) Role of the histone 'tails' in the folding of oligonucleosomes depleted of histone H1, J. Biol. Chem 267, 19587-19595.
67. Karantza, V., Freire, E., and Moudrianakis, E. N. (2001) Thermodynamic studies of the core histones: stability of the octamer subunits is not altered by removal of their terminal domains, Biochemistry 40, 13113-13123.
68. Toth, K. F., Mazurkiewicz, J., and Rippe, K. (2005) Association states of nucleosome assembly protein 1 and its complexes with histones, J. Biol. Chem. 280, 15690-15699.
69. Park, Y.-J., and Luger, K. (2006) The structure of nucleosome assembly protein 1, Proc. Natl. Acad. Sci. U.S.A. 103, 1248-1253.
70. Decanniere, K., Babu, A. M., Sandman, K., Reeve, J. N., and Heinemann, U. (2000) Crystal structures of recombinant histones HMfA and HMfB from the hyperthermophilic archaeon Methanothermus fervidus, J. Mol. Biol. 303, 35-47.
71. Marc, F., Sandman, K., Lurz, R., and Reeve, J. N. (2002) Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling, J. Biol. Chem. 277, 30879-30886.
72. Baneres, J.-L., Martin, A., and Parello, J. (1997) The N tails of histones H3 and H4 adopt a highly structured conformation in the nucleosome, J. Mol. Biol. 273, 503-508.
73. Wang, X., Moore, S. C., Laszckzak, M., and Ausio, J. (2000) Acetylation increases the alpha-helical content of the histone tails of the nucleosome, J. Biol. Chem. 275, 35013-35020.
74. Sivolob, A., De Lucia, F., Alilat, M., and Prunell, A. (2000) Nucleosome dynamics. VI. Histone tail regulation of tetrasome chiral transition: a relaxation study of tetrasomes on DNA mincircles, J. Mol. Biol. 295, 55-69.
75. Morales, V., and Richard-Foy, H. (2000) Role of histone N-terminal tails and their acetylation in nucleosome dynamics, Mol. Cell. Biol. 20, 7230-7237.
76. Gavin, I., Horn, P. J., and Peterson, C. L. (2001) SWI/SNF chromatin remodeling requires changes in DNA topology, Mol. Cell 7, 97-104.
77. Lia, G., Praly, E., Ferreira, H., Stockdale, C., Tse-Dinh, Y. C., Dunlap, D., Croquette, V., Bensimon, D., and Owen-Hughes, T. (2006) Direct observation of DNA distortion by the RSC complex, Mol. Cell 21, 417-425.
78. Droge, P. (1994) Protein tracking-induced supercoiling of DNA: a tool to regulate DNA transactions in vivo? Bioassays 16, 91-99.